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Life Span Extension of Drosophila Melanogaster: Genetic and Population Studies Lawrence G University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Lawrence G. Harshman Publications Papers in the Biological Sciences 2003 Life Span Extension of Drosophila melanogaster: Genetic and Population Studies Lawrence G. Harshman University of Nebraska–Lincoln, [email protected] Follow this and additional works at: http://digitalcommons.unl.edu/biosciharshman Part of the Entomology Commons, Genetics Commons, and the Gerontology Commons Harshman, Lawrence G., "Life Span Extension of Drosophila melanogaster: Genetic and Population Studies" (2003). Lawrence G. Harshman Publications. 27. http://digitalcommons.unl.edu/biosciharshman/27 This Article is brought to you for free and open access by the Papers in the Biological Sciences at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Lawrence G. Harshman Publications by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Published in Population and Development Review 29, Supplement: Life Span: Evolutionary, Ecological, and Demographic Perspectives (2003), pp. 99–126. Copyright © 2003 The Population Council, Inc. Used by permission. Life Span Extension of Drosophila melanogaster: Genetic and Population Studies Lawrence G. Harshman During the past two decades, genetic studies of model organisms have been the most im- portant tool underlying advances in understanding the biological basis of aging and lon- gevity. Drosophila melanogaster, the geneticist's "fruit fly," is a model organism because it has been the focus of genetic studies for more than 90 years. This review argues that studies on D. melanogaster will make an especially important contribution to the field of aging and longevity at the intersection of research on genetics, complex traits, and fly populations. Five approaches have been used to study the genetics of longevity of D. melanogaster: (1) laboratory selection, (2) quantitative genetics, (3) transgenic overexpression, (4) muta- tion analysis, and (5) measurement of gene expression. The first two approaches attempt to decompose longevity as a complex character. The third and fourth approaches start by looking for major gene effects on life span. The fifth approach is emerging as part of a major advance in technology in which the expression of almost all genes in the genome can be measured at one time. Genetic research on aging and longevity using D. melanogaster has been reviewed pre- viously (Arking 1987, 1988; Arking and Dudas 1989; Rose 1991; Curtsinger et al. 1995; Tower 1996; Stearns and Partridge 2001). The present chapter reviews the range of genetic approaches used to study aging and life span (length of life). Selection experiments in the laboratory Natural selection has shaped organic evolution whereas artificial selection is a human en- deavor, usually with some utilitarian goal. Artificial selection is typically conducted on H ARSHMAN, P OPULATION AND D EVELOPMENT R EVIEW 29S (2003) complex traits that are controlled by multiple genes. Generation by generation, artificial selection can progressively change the mean value of a complex trait, such as longevity, in a population. The genes that underlie the response to selection, and traits that change as correlated responses to selection, are of interest in the context of understanding aging and longevity. Figure 1 shows the distribution of a trait in a population of individuals undergoing se- lection. When individuals from the distribution are nonrepresentatively selected to con- tribute to the next generation and genetic variation contributes to the trait variation in the population, there can be a genetic-based change in the mean value of the trait in the next generation. Figure 1. The distribution of a trait and population mean (μ) Notes: (A) The mean of the subset of individuals used to propagate the next generation is μs,. Selection intensity (S) is a function of the difference between μ and μs. (B) The response (R) to selection is defined in terms of the mean trait value in the next generation (μ′) and the previous generation (μ). Source: Hartl and Clark 1997. Artificial or natural selection in the laboratory has been used to study a range of traits (Rose 1984; Hoffmann and Parsons 1989; Rose et al. 1990; Huey and Kingsolver 1993; Rose et al. 1996; Gibbs 1999). Selection experiments magnify the difference between selected populations and ancestral or unselected control populations. Large differences are easier to study; selection experiments facilitate investigation by increasing the signal-to-noise ra- tio in the comparison of selected and control (unselected) populations. 2 H ARSHMAN, P OPULATION AND D EVELOPMENT R EVIEW 29S (2003) The direct response to selection is the change in the trait targeted for selection. The in- direct responses to selection consist of changes in other traits. Indirect responses to selec- tion can be informative because they indicate genetic correlations between traits. Such cor- relations can reveal traits whose association with the directly selected trait was not antici- pated at the beginning of the experiment. Moreover, genetic associations between traits can provide circumstantial evidence about mechanisms underlying the direct response to selection. For example, negative correlations between traits in selection experiments sug- gest tradeoffs (Rose et al. 1990). Tradeoffs are based on constraints involving energy, space, hormones, or structural biology such that an increase in the expression of one trait results in a decrease in another trait. Tradeoffs are a pivotal consideration in the evolution of lon- gevity and other life-history traits (Williams 1957; Stearns 1989, 1992; Reznick 1985; Zera and Harshman 2001). A great deal of D. melanogaster genetic research on longevity has been based on artificial selection in the laboratory. The following summary of a subset of results is designed to focus on general outcomes and provide perspective on the pluses and minuses associated with the use of selection experiments to study aging and longevity. Selection experiments on life span Although not the first studies of this genre, two artificial selection experiments have had a long-term impact on the field (Rose 1984; Luckinbill et al. 1984). In each case, the mode of selection was to select flies to propagate the next generation using individuals that re- mained fertile at old ages. For example, an artificial selection experiment by Rose (1984) increased the age of breeding from 4-day-old adults to 28 days (generation 1), then to 35 days (generations 2 and 3), then to 42 days, and ultimately used 70-day-old adults to main- tain the selected lines. The important features of the experimental design included a high degree of replication (5 selected and 5 control lines), a relatively large population size in each line to mitigate inbreeding, and a laboratory-adapted ancestral population (Rose 1984; Rose et al. 1996). The control lines were maintained using the same generation time as the ancestral population, meaning that the breeders for the next generation were young adults. Rose (1984) and Luckinbill et al. (1984) substantially increased longevity (by 50 to 100 per- cent) in their selected lines. Research on their lines highlighted stress resistance as a genetic correlate of longevity. Selection experiments provided initial evidence for a genetic relationship between stress resistance and longevity. Relative to control lines, the Rose lines, selected for longevity, were resistant to starvation, desiccation, and ethanol fumes, as well as elevated tempera- ture under some conditions (Service et al. 1985). The Luckinbill set of lines provided the first evidence for a genetic correlation between longevity and oxidative stress resistance (Arking et al. 1991). This observation was particularly significant because it provided in- direct support for the free radical theory of aging (Harman 1956), a predominant biochem- ical hypothesis that explains aging in terms of oxidative damage to macromolecules in cells (Wallace 1992; Martin et al. 1996; Johnson et al. 1999; Guarente and Kenyon 2000). Selection experiments also provided early evidence for a genetic association between early-age reproduction and longevity. Females from control populations exhibited a rela- tively short life span and high early-age egg production, but the converse was observed 3 H ARSHMAN, P OPULATION AND D EVELOPMENT R EVIEW 29S (2003) for the lines selected for extended longevity (Rose 1984). Selected-line females were less fecund early in life regardless of whether they had mated or were virgin (Service 1989). Selected-line males also exhibited reduced reproductive function early in life compared to control-line males (Service and Fales 1993; Service and Vossbrink 1996). During the course of many generations of selection, however, early-age egg production evolved to become higher in the selected than in the control lines in some environments (Leroi et al. 1994). This outcome was interesting from an evolutionary standpoint, but it raises questions about the utility of the selection experiment approach because some results can be incon- sistent over time. Ancillary selection experiments have been used to test the direct and correlated re- sponses to selection. For example, direct selection for starvation resistance resulted in flies with extended longevity (Rose et al. 1992). However, Harshman et al. (1999) selected only for female starvation resistance and did not observe an increase in female or male longev- ity.
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